Prefrontal-Hippocampal Coupling During Memory Processing Is Modulated by COMT Val158Met Genotype

Biological Psychiatry

Volumn 60, Issue 11, 2006, Pages 1250-1258

  Bertolino, Alessandro ^a,b,d   Rubino, Valeria ^a   Sambataro, Fabio ^a,b   Blasi, Giuseppe ^a   Latorre, Valeria ^a   Fazio, Leonardo ^a   Caforio, Grazia ^a   Petruzzella, Vittoria ^c   Kolachana, Bhaskar ^b   Hariri, Ahmad ^b   Meyer Lindenberg, Andreas ^b   Nardini, Marcello ^a   Weinberger, Daniel R ^b   Scarabino, Tommaso ^d  

^a Section on Mental Disorders   (Italy)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c UNIVERSITY OF BARI   (Italy)

^d IRCCSS Casa Sollievo della Sofferenza ^*  (Italy)

Author keywords

COMT val158met; connectivity; declarative memory; dopamine; hippocampus; prefrontal cortex

Indexed keywords

CATECHOL METHYLTRANSFERASE; DOPAMINE; METHIONINE; VALINE;

ADULT; ALLELE; ARTICLE; DEMOGRAPHY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY; MEMORY CONSOLIDATION; NERVE CELL NETWORK; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RECOGNITION; REFLEX RECRUITMENT;

ADULT; ANALYSIS OF VARIANCE; CATECHOL O-METHYLTRANSFERASE; COHORT STUDIES; FEMALE; GENOTYPE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; MALE; MENTAL RECALL; METHIONINE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PREFRONTAL CORTEX; RECOGNITION (PSYCHOLOGY); VALINE;

EID: 33748944189     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2006.03.078     Document Type: Article

References (69)

1. Adolphs R., Cahill L., Schul R., and Babinsky R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn Mem 4 (1997) 291-300
2. Bertolino A., Blasi G., Latorre V., Rubino V., Rampino A., Sinibaldi L., et al. Additive effects of genetic variation in dopamine regulating genes on working memory cortical activity in human brain. J Neurosci 26 (2006) 3918-3922
3. Bertolino A., Caforio G., Blasi G., De Candia M., Latorre V., Petruzzella V., et al. Interaction of COMT Val108/158 Met genotype and olanzapine treatment on prefrontal cortical function in patients with schizophrenia. Am J Psychiatry 161 (2004) 1798-1805
4. Bertolino A., Nawroz S., Mattay V.S., Barnett A.S., Duyn J.H., Moonen C.T., et al. Regionally specific pattern of neurochemical pathology in schizophrenia as assessed by multislice proton magnetic resonance spectroscopic imaging. Am J Psychiatry 153 (1996) 1554-1563
5. Bertolino A., Roffman J.L., Lipska B.K., van Gelderen P., Olson A., and Weinberger D.R. Reduced N-acetylaspartate in prefrontal cortex of adult rats with neonatal hippocampal damage. Cereb Cortex 12 (2002) 983-990
6. Bertolino A., Saunders R.C., Mattay V.S., Bachevalier J., Frank J.A., and Weinberger D.R. Altered development of prefrontal neurons in rhesus monkeys with neonatal mesial temporo-limbic lesions: A proton magnetic resonance spectroscopic imaging study. Cereb Cortex 7 (1997) 740-748
7. Bilder R.M., Volavka J., Lachman H.M., and Grace A.A. The catechol-O-methyltransferase polymorphism: Relations to the tonic-phasic dopamine hypothesis and neuropsychiatric phenotypes. Neuropsychopharmacology 29 (2004) 1943-1961
8. Birn R.M., Cox R.W., and Bandettini P.A. Detection versus estimation in event-related fMRI: Choosing the optimal stimulus timing. Neuroimage 15 (2002) 252-264
9. Blasi G., Mattay V.S., Bertolino A., Elvevag B., Callicott J.H., Das S., et al. Effect of catechol-O-methyltransferase val158met genotype on attentional control. J Neurosci 25 (2005) 5038-5045
10. Bookheimer S.Y., Strojwas M.H., Cohen M.S., Saunders A.M., Pericak-Vance M.A., Mazziotta J.C., et al. Patterns of brain activation in people at risk for Alzheimer's disease. N Engl J Med 343 (2000) 450-456
11. Buckner R.L., Petersen S.E., Ojemann J.G., Miezin F.M., Squire L.R., and Raichle M.E. Functional anatomical studies of explicit and implicit memory retrieval tasks. J Neurosci 15 (1995) 12-29
12. Burdick K.E., Lencz T., Funke B., Finn C.T., Szeszko P.R., Kane J.M., et al. Genetic variation in DTNBP1 influences general cognitive ability. Hum Mol Genet 15 (2006) 1563-1568
13. Carr D.B., and Sesack S.R. Hippocampal afferents to the rat prefrontal cortex: Synaptic targets and relation to dopamine terminals. J Comp Neurol 369 (1996) 1-15
14. Chen J., Lipska B.K., Halim N., Ma Q.D., Matsumoto M., Melhem S., et al. Functional analysis of genetic variation in catechol-O-methyltransferase (COMT): effects on mRNA, protein, and enzyme activity in postmortem human brain. Am J Hum Genet 75 (2004) 807-821
15. de Frias C.M., Annerbrink K., Westberg L., Eriksson E., Adolfsson R., and Nilsson L.G. COMT gene polymorphism is associated with declarative memory in adulthood and old age. Behav Genet 34 (2004) 533-539
16. Diaz-Asper C.M., Weinberger D.R., and Goldberg T.E. Catechol-O-methyltransferase polymorphisms and some implications for cognitive therapeutics. NeuroRx 3 (2006) 97-105
17. Durstewitz D., Seamans J.K., and Sejnowski T.J. Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83 (2000) 1733-1750
18. Egan M.F., Goldberg T.E., Kolachana B.S., Callicott J.H., Mazzanti C.M., Straub R.E., et al. Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia. Proc Natl Acad Sci U S A 98 (2001) 6917-6922
19. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112 (2003) 257-269
20. Fernandez G., and Tendolkar I. Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: Human declarative memory formation at the system level. Brain Res Bull 55 (2001) 1-9
21. Floresco S.B., and Grace A.A. Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. J Neurosci 23 (2003) 3930-3943
22. Floresco S.B., West A.R., Ash B., Moore H., and Grace A.A. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6 (2003) 968-973
23. Frey U., Schroeder H., and Matthies H. Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Res 522 (1990) 69-75
24. Friston K.J., Holmes A.P., and Worsley K.J. How many subjects constitute a study?. Neuroimage 10 (1999) 1-5
25. Gabrieli J.D., Brewer J.B., Desmond J.E., and Glover G.H. Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276 (1997) 264-266
26. Gabrieli J.D., Poldrack R.A., and Desmond J.E. The role of left prefrontal cortex in language and memory. Proc Natl Acad Sci U S A 95 (1998) 906-913
27. Gaffan D., and Harrison S. Inferotemporal-frontal disconnection and fornix transection in visuomotor conditional learning by monkeys. Behav Brain Res 31 (1988) 149-163
28. Gogos J.A., Morgan M., Luine V., Santha M., Ogawa S., Pfaff D., et al. Catechol-O-methyltransferase-deficient mice exhibit sexually dimorphic changes in catecholamine levels and behavior. Proc Natl Acad Sci U S A 95 (1998) 9991-9996
29. Hariri A.R., Goldberg T.E., Mattay V.S., Kolachana B.S., Callicott J.H., Egan M.F., et al. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J Neurosci 23 (2003) 6690-6694
30. Harrison P.J., and Weinberger D.R. Schizophrenia genes, gene expression, and neuropathology: On the matter of their convergence. image 5. Mol Psychiatry 10 (2005) 40-68
31. Heckers S., Rauch S.L., Goff D., Savage C.R., Schacter D.L., Fischman A.J., et al. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat Neurosci 1 (1998) 318-323
32. Jay T.M., Burette F., and Laroche S. NMDA receptor-dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat. Eur J Neurosci 7 (1995) 247-250
33. Karoum F., Chrapusta S.J., Egan M.F., and Wyatt R.J. Absence of 6-hydroxydopamine in the rat brain after treatment with stimulants and other dopaminergic agents: A mass fragmentographic study. J Neurochem 61 (1993) 1369-1375
34. Kelley W.M., Miezin F.M., McDermott K.B., Buckner R.L., Raichle M.E., Cohen N.J., et al. Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron 20 (1998) 927-936
35. Kirchhoff B.A., Wagner A.D., Maril A., and Stern C.E. Prefrontal-temporal circuitry for episodic encoding and subsequent memory. J Neurosci 20 (2000) 6173-6180
36. Lang P.J., Bradley M.M., and Cuthbert B.N. International Affective Picture (1997)
37. System (IAPS): Technical manual and affective ratings. Gainesville, FL: NIMH Center for the Study of Emotion and Attention, University of Florida.•••
38. Lena I., Dh tel H., Garbay C., and Dauge V. Involvement of D2 dopamine receptors in the opposing effects of two CCK-B agonists in a spatial recognition memory task: Role of the anterior nucleus accumbens. Psychopharmacology (Berl) 153 (2001) 170-179
39. Levine B., Black S.E., Cabeza R., Sinden M., McIntosh A.R., Toth J.P., et al. Episodic memory and the self in a case of isolated retrograde amnesia. Brain 121 Pt 10 (1998) 1951-1973
40. Li S., Cullen W.K., Anwyl R., and Rowan M.J. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 6 (2003) 526-531
41. Manahan-Vaughan D., and Kulla A. Regulation of depotentiation and long-term potentiation in the dentate gyrus of freely moving rats by dopamine D2-like receptors. Cereb Cortex 13 (2003) 123-135
42. Markowitsch H.J., and Kessler J. Massive impairment in executive functions with partial preservation of other cognitive functions: the case of a young patient with severe degeneration of the prefrontal cortex. Exp Brain Res 133 (2000) 94-102
43. Matsumoto M., Weickert C.S., Akil M., Lipska B.K., Hyde T.M., Herman M.M., et al. Catechol O-methyltransferase mRNA expression in human and rat brain: Evidence for a role in cortical neuronal function. Neuroscience 116 (2003) 127-137
44. Mattay V.S., Goldberg T.E., Fera F., Hariri A.R., Tessitore A., Egan M.F., et al. Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proc Natl Acad Sci U S A 100 (2003) 6186-6191
45. Meyer-Lindenberg A.S., Olsen R.K., Kohn P.D., Brown T., Egan M.F., Weinberger D.R., et al. Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Arch Gen Psychiatry 62 (2005) 379-386
46. Mulder A.B., Arts M.P., and Lopes da Silva F.H. Short- and long-term plasticity of the hippocampus to nucleus accumbens and prefrontal cortex pathways in the rat, in vivo. Eur J Neurosci 9 (1997) 1603-1611
47. Passingham R.E., Toni I., and Rushworth M.F. Specialisation within the prefrontal cortex: The ventral prefrontal cortex and associative learning. Exp Brain Res 133 (2000) 103-113
48. Peleg-Raibstein D., Pezze M.A., Ferger B., Zhang W.N., Murphy C.A., Feldon J., et al. Activation of dopaminergic neurotransmission in the medial prefrontal cortex by N-methyl-d-aspartate stimulation of the ventral hippocampus in rats. Neuroscience 132 (2005) 219-232
49. Petrides M. Frontal lobes and working memory, evidence from the investigations of the effects of cortical excisions in nonhuman primates. In: Boller F., and Grafman J. (Eds). Handbook of Neuropsychology vol. 10 (1995), Elsevier, Amsterdam 59-81
50. Petrides M. The mid-ventrolateral prefrontal cortex and active mnemonic retrieval. Neurobiol Learn Mem 78 (2002) 528-538
51. Pezawas L., Meyer-Lindenberg A., Drabant E.M., Verchinski B.A., Munoz K.E., Kolachana B.S., et al. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: A genetic susceptibility mechanism for depression. Nat Neurosci 8 (2005) 828-834
52. Poldrack R.A., Prabhakaran V., Seger C.A., and Gabrieli J.D. Striatal activation during acquisition of a cognitive skill. Neuropsychology 13 (1999) 564-574
53. Ranganath C., Cohen M.X., Dam C., and D'Esposito M. Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. J Neurosci 24 (2004) 3917-3925
54. Rosene D.L., and Van Hoesen G.W. Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198 (1977) 315-317
55. Sawaguchi T., and Goldman-Rakic P.S. The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. J Neurophysiol 71 (1994) 515-528
56. Sawaguchi T., and Goldman-Rakic P.S. The role of D1-dopamine receptor in working memory: Local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. J Neurophysiol 71 (1994) 515-528
57. Schacter D.L., and Wagner A.D. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 9 (1999) 7-24
58. Seamans J.K., Floresco S.B., and Phillips A.G. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. J Neurosci 18 (1998) 1613-1621
59. Seamans J.K., Gorelova N., Durstewitz D., and Yang C.R. Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21 (2001) 3628-3638
60. Seamans J.K., and Yang C.R. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74 (2004) 1-58
61. Smolka M.N., Schumann G., Wrase J., Grusser S.M., Flor H., Mann K., et al. Catechol-O-methyltransferase val158met genotype affects processing of emotional stimuli in the amygdala and prefrontal cortex. J Neurosci 25 (2005) 836-842
62. Thierry A.M., Gioanni Y., Degenetais E., and Glowinski J. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 10 (2000) 411-419
63. Wagner A.D., Desmond J.E., Glover G.H., and Gabrieli J.D. Prefrontal cortex and recognition memory. Functional-MRI evidence for context-dependent retrieval processes. Brain 121 Pt 10 (1998) 1985-2002
64. Wagner A.D., Koutstaal W., and Schacter D.L. When encoding yields remembering: Insights from event-related neuroimaging. Philos Trans R Soc Lond B Biol Sci 354 (1999) 1307-1324
65. Wagner A.D., Pare-Blagoev E.J., Clark J., and Poldrack R.A. Recovering meaning: Left prefrontal cortex guides controlled semantic retrieval. Neuron 31 (2001) 329-338
66. Wagner A.D., Poldrack R.A., Eldridge L.L., Desmond J.E., Glover G.H., and Gabrieli J.D. Material-specific lateralization of prefrontal activation during episodic encoding and retrieval. Neuroreport 9 (1998) 3711-377
67. Wagner A.D., Schacter D.L., Rotte M., Koutstaal W., Maril A., Dale A.M., et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281 (1998) 1188-1191
68. Winterer G., and Weinberger D.R. Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci 27 (2004) 683-690
69. Zeineh M.M., Engel S.A., Thompson P.M., and Bookheimer S.Y. Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science 299 (2003) 577-580